A bacterial metapopulation adapts locally to phage predation despite global dispersal

Abstract

Using a combination of bacterial and phage-targeted metagenomics, we analyzed two geographically remote sludge bioreactors enriched in a single bacterial species Candidatus Accumulibacter phosphatis (CAP). We inferred unrestricted global movement of this species and identified aquatic ecosystems as the primary environmental reservoirs facilitating dispersal. Highly related and geographically remote CAP strains differed principally in genomic regions encoding phage defense mechanisms. We found that CAP populations were high density, clonal, and nonrecombining, providing natural targets for "kill-the-winner" phage predation. Community expression analysis demonstrated that phages were consistently active in the bioreactor community. Genomic signatures linking CAP to past phage exposures were observed mostly between local phage and host. We conclude that CAP strains disperse globally but must adapt to phage predation pressure locally.

Figure 1.

Gene phylogenies reconstructed using nucleotide sequence show geographic intermingling of CAP strains. Sequences obtained from the US and OZ samples are shown in red and blue, respectively. Asterisks mark dominant strains. IMG (Markowitz et al. 2006) gene object identifiers (beginning with 2000) are given for genes derived from metagenomic data. Support for interior nodes are indicated by bootstrap resampling percentages. The following trees are shown. (A) Polyphosphate kinase (PCR-amplified clones begin with BPBW); (B) Ribosomal protein L9; (C) holiday junction resolvase, DNA-binding subunit RuvA. Schematics are provided for reference to show the expected tree topologies for endemic (D) and freely migrating (E) populations. Note that in the latter case, high recombination frequencies between local and introduced strains may mask dispersal patterns.

Figure 2.

Sample alignments of homologous regions in the dominant US and OZ strains showing substitution (A) and insertion (B) of CRISPR elements. CRISPR repeats are indicated by sets of vertical bars with colors denoting different repeat sequences. Total number of repeats for each CRISPR element is unknown because of incomplete sequence information in the draft assembly; therefore, a minimum estimate is given. (C) Schematic magnification of dominant CAP CRISPR element and a contig from the phage virion metagenome revealing a phage that has previously infected CAP. All spacers targeting the phage had the same orientation. The starting positions of each spacer and the matching segments in the phage are indicated. The drawing is not to scale, and the actual number of repeats is significantly higher.